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. 2024 Nov 17;245(2):458–464. doi: 10.1111/nph.20251

Origins of xyloglucan‐degrading enzymes in fungi

Emily D Trudeau 1,✉, Harry Brumer 1,2, Mary L Berbee 1,✉
PMCID: PMC11655419  PMID: 39550623

Summary

The origin story of land plants – the pivotal evolutionary event that paved the way for terrestrial ecosystems of today to flourish – lies within their closest living relatives: the streptophyte algae. Streptophyte cell wall composition has evolved such that profiles of cell wall polysaccharides can be used as taxonomic markers. Since xyloglucan is restricted to the streptophyte lineage, we hypothesized that fungal enzymes evolved in response to xyloglucan availability in streptophyte algal or land plant cell walls. The record of the origins of these enzymes is embedded in fungal genomes, and comparing genomes of fungi that share an ancient common ancestor can provide insights into fungal interactions with early plants. This Viewpoint contributes a review of evidence underlying current assumptions about the distribution of xyloglucan in plant and algal cell walls. We evaluate evolutionary scenarios that may have given rise to the observed distribution of putative xyloglucanases in fungi and discuss possible biological contexts in which these enzymes could have evolved. Our findings suggest that fungal xyloglucanase evolution was more likely driven by land plant diversification and biomass accumulation than by the first origins of xyloglucan in streptophyte algal cell walls.

Keywords: carbohydrate‐active enzymes, early evolution, plant cell wall, plant–fungus interactions, streptophyte algae, xyloglucan, xyloglucanases

Introduction

Fungi have coexisted with land plants and their algal predecessors for hundreds of millions of years. Through their interactions with plants, fungi have shaped the world in consequential ways and may have played a pivotal role in the very development of early terrestrial ecosystems (Delaux & Schornack, 2021). Whether plant–fungus associations existed in aquatic ecosystems before plant terrestrialization remains unknown from the fossil record alone (Strullu‐Derrien et al., 2018; Berbee et al., 2020). Comparative phylogenetic approaches, focusing on genes involved in plant–fungus interactions, can provide evidence for interdependence between ancient fungi and plants (Berbee et al., 2020; Trudeau & Berbee, 2024). To interact with plants and take up nutrients, fungi secrete enzymes that breakdown plant cell wall polysaccharides – cellulose, hemicelluloses, and pectins. However, composition of the plant cell wall has evolved over evolutionary time such that profiles of cell wall polysaccharides can be used as taxonomic markers (Popper & Tuohy, 2010). Reconciling evolutionary histories of fungal enzymes with the appearance of different cell wall components in early plants provides a framework for inferring ancient plant–fungus interactions.

To apply this framework, we must look at cell wall components that may be restricted to land plants and their closest relatives, the streptophyte algae. One such polysaccharide is xyloglucan (XyG), a major matrix glycan in most primary plant cell walls that binds to cellulose and plays a role in wall structure and mechanics (Cosgrove, 2022). In primary walls of dicots, XyG is the most abundant hemicellulose, comprising 20–25% of the cell wall by weight (Pauly & Keegstra, 2016). XyG also acts as a seed storage polysaccharide in some species (Buckeridge et al., 2000) and is released by the roots and rhizoids of land plants, acting in soil particle aggregation and formation (Galloway et al., 2018). XyG is composed of a β‐(1,4)‐d‐glucan backbone decorated with various sidechains (Fig. 1a). These sidechains characteristically start with α‐(1,6)‐d‐xylosyl residues, which can be further decorated with additional glycosides of galactose, fucose, arabinose, and uronic acids (Pauly & Keegstra, 2016). Presence of XyG in the cell wall and its structure are dynamic, varying across species, tissue types, and developmental stages within a single plant (Fangel et al., 2012; Shtein et al., 2018).

Fig. 1.

(a) Diagram of typical xyloglucan structure. (b) Cladogram of plant and algal lineages with a table showing type of evidence for xyloglucan in each taxon.

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Evidence for xyloglucan (XyG) in plant and algal cell walls. (a) Representative dicot XyG structure with one‐letter codes denoting substitution patterns of each backbone residue (see Pauly & Keegstra, 2016 for a full description of subunit identifiers and alternative structures observed in diverse plant taxa). (b) Phylogenetic relationships within the plant lineage showing types of evidence for XyG in cell walls. XyG may have evolved in an early shared ancestor of Klebsormidiophyceae and land plants (c. 1090 million years ago (Ma), stem age), and was probably present in the last common ancestor of Zygnematophyceae and land plants (c. 720 Ma, crown age) (Bowles et al., 2024).

Reviewing evidence for xyloglucan in plant cell walls

Evolutionary origins of fungal xyloglucanases – xyloglucan‐specific endo‐β‐1,4‐glucanases, EC 3.2.1.151 (Eklöf et al., 2012) – must be placed in context of when their substrates became available. Inferring when XyG first appeared in plant cell walls requires a comprehensive survey of cell wall composition in extant taxa. Where XyG is present in cell walls of descendants of a common ancestor, we assume the last common ancestor (LCA) also shared this trait. Potential for XyG biosynthesis can be assessed bioinformatically, but experimental approaches – including carbohydrate microarrays, in situ immunolabeling, biochemical analysis by enzymatic digestion, and fine‐structure mapping by NMR spectroscopy or mass spectrometry – are required to detect presence of XyG in the cell wall (Fangel et al., 2012). Here, we require both molecular and experimental evidence to infer origins of XyG within plant evolution.

Evidence for XyG or its biosynthetic machinery has not been reported in prasinodermophyte (Li et al., 2020; Bachy et al., 2022), glaucophyte (Popper et al., 2011; Han et al., 2019), or rhodophyte algae (Ulvskov et al., 2013; Synytsya et al., 2015; Fig. 1b). Chlorophyte algae lack almost all XyG‐related genes (Del Bem & Vincentz, 2010) and chlorophyte cell wall composition remains poorly characterized (Domozych & LoRicco, 2024). A polysaccharide with d‐xylose β‐1,4‐linked to d‐glucose has been reported from cell walls of the chlorophyte Ulva lactuca (Lahaye et al., 1994), though structurally this is not a canonical XyG (Fig. 1a). As such, the characterized classes of xyloglucanases discussed below cannot be assumed to exhibit activity toward this polysaccharide, and we exclude it from further consideration.

Streptophyte algae are divided into two paraphyletic groups: the earlier‐diverging KCM‐grade (Klebsormidiophyceae, Chlorokybophyceae and Mesostigmatophyceae), and the later‐diverging ZCC‐grade (Zygnematophyceae, Coleochaetophyceae, and Charophyceae) (Wickett et al., 2014; Fürst‐Jansen et al., 2020). Streptophytes in the earliest‐diverging Chlorokybophyceae and Mesostigmatophyceae lack the majority of genes related to XyG biosynthesis (Del‐Bem, 2018; Wang et al., 2020; Feng et al., 2024). Carbohydrate microarrays probed with XyG‐specific antibodies did not show labelling in Chlorokybus, though a low signal was observed in Mesostigma (Sørensen et al., 2011; Mikkelsen et al., 2021). The Klebsormidiophyceae possess homologs of all known enzymes involved in XyG biosynthesis (Del‐Bem, 2018) and XyG epitopes have been detected with immunolabeling (Herburger et al., 2018). However, carbohydrate microarrays did not show XyG labelling in Klebsormidium (Sørensen et al., 2011; Mikkelsen et al., 2021), nor was it detected biochemically by enzymatic digestion (Popper & Fry, 2003).

Members of the later‐diverging Zygnematophyceae, Coleochaetophyceae, and Charophyceae have been shown to have XyG by carbohydrate microarrays and immunolabeling studies, by fine‐structure mapping in the case of Coleochaetophyceae and Zygnematophyceae, and by biochemical analysis for Zygnematophyceae (Domozych et al., 2009; Sørensen et al., 2011; Mikkelsen et al., 2021). With XyG ubiquitous in cell walls of most bryophytes and vascular plants (Popper & Fry, 2003; Peña et al., 2008; Hsieh & Harris, 2012; Leroux et al., 2015; Henry et al., 2020), our estimate of possible origins of cell wall XyG is in the lineage giving rise to Klebsormidiophyceae and land plants. However, the possibility of antibodies binding to epitopes in polymers other than XyG cannot be excluded completely (Popper & Tuohy, 2010), and as a result some consider biochemical detection to be necessary for confirming XyG presence in cell walls (Franková & Fry, 2021). Therefore, we propose that XyG may have appeared, at the earliest, in a shared ancestor of Klebsormidiophyceae and land plants, and was probably present in the LCA of Zygnematophyceae and land plants, corresponding to a window of c. 1090–720 million years ago (Ma) (Bowles et al., 2024).

Distribution of xyloglucanase genes in fungi

Since XyG likely originated within the streptophyte lineage, xyloglucanase genes can be used as markers to infer potential interactions between fungi and xyloglucan‐containing streptophytes. Breakdown of XyG first involves depolymerization of the polysaccharide backbone into smaller fragments by glycoside hydrolases (GHs) with endo‐β‐1,4‐glucanase activity (Attia & Brumer, 2016). While some glucanases can hydrolyze both cellulose and xyloglucan, others are xyloglucan‐specific and are designated as xyloglucanases (Matsuzawa et al., 2021). Enzymes that degrade and modify carbohydrates have been classified into sequence‐based families according to their structurally related catalytic domains by the CAZy (Carbohydrate‐Active enZymes) database (http://www.cazy.org/) (Drula et al., 2022). In fungi, the three main families of glycoside hydrolases that harbor xyloglucanase enzymes are: GH5 subfamily 4 (GH5_4), GH44, and GH74 (Gilbert et al., 2008; Aspeborg et al., 2012; Arnal et al., 2019). To investigate the distribution of putative xyloglucanases in fungi (Fig. 2), we searched annotated genomes in JGI MycoCosm (Grigoriev et al., 2014) and conducted Blastp searches (e‐value < e −10) (Altschul et al., 1990) using characterized sequences from the CAZy database as queries.

Fig. 2.

A cladogram spanning the fungal kingdom with pie charts at internal nodes, representing marginal ancestral state reconstructions for each enzyme family.

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Inferred origins of xyloglucan‐degrading enzymes in fungi. Phylogenetic relationships between the fungi with marginal ancestral state reconstructions for GH5_4 (yellow), GH44 (blue), and GH74 (green) families shown on nodes. Occurrence of each gene family in terminal taxa is shown at tips. Species tree and branch lengths adapted from Amses et al. (2022) and Chang et al. (2021), with placements of class and order level nodes derived from Prieto & Wedin, scenario 3 (2013) for Ascomycota and Zhao et al. (2017) for Basidiomycota. GH, glycoside hydrolase; LCA, last common ancestor.

GH5_4 members (http://www.cazy.org/GH5_4_characterized.html) occur across subphylum Pezizomycotina in Ascomycota and have been biochemically characterized in a few taxa (Liu et al., 2013; Matsuzawa et al., 2020), but within Basidiomycota they are restricted to only one species in order Agaricales (Flagelloscypha, a root endophyte) and to the Cantharellales, an order rich in root‐associated fungi, including several symbionts of orchids (Selosse et al., 2022). They are also found in the anaerobic gut fungi in Neocallimastigomycetes and are predicted to occur in a small subset of the semi‐aquatic Chytridiomycetes in phylum Chytridiomycota.

GH44 members (http://www.cazy.org/GH44_characterized.html) have been experimentally characterized in class Agaricomycetes (Basidiomycota) and were previously thought to be restricted to this phylum (Sun et al., 2022). However, putative homologs can be found in Chytridiomycota, though are absent from Ascomycota.

GH74 members (http://www.cazy.org/GH74_characterized.html) are present in Basidiomycota and Ascomycota and have been experimentally characterized in both phyla (Hasper et al., 2002; Ishida et al., 2007). Putative GH74 genes can also be found in Mucoromycota and Chytridiomycota.

Notably, xyloglucanases are not known from phylum Zoopagomycota, indicating that if these plant‐degrading enzymes were present in a common ancestor, they have been lost in taxa that evolved to parasitize animals and other fungi.

When did fungi begin degrading xyloglucan?

To infer origins of xyloglucanases in fungi, we conducted marginal ancestral state reconstruction using phytools in R (Revell, 2012; R Core Team, 2021) under an equal‐rates model with a representative sampling of fungi and other eukaryotes as outgroups. We used a relative likelihood threshold of 75% to infer likely character states at ancestral nodes and took continued retention into consideration in addition to point estimates of origins. For all gene families, our analysis points to independent evolution of fungal xyloglucanases within phyla that was more likely driven by an increase in quantity of XyG than by its first origins (Fig. 2).

Relative likelihoods support multiple gains of xyloglucanase genes: in the ancestor of Agaricomycetes, in the ancestor of Pezizomycotina, and in various lineages in Chytridiomycota, implying the c. 750 Ma LCA of Dikarya and Chytridiomycota lacked xyloglucanases. Nodes corresponding to the common ancestor of Agaricomycetes and the common ancestor of Pezizomycotina are dated at c. 310 and 330 Ma, respectively (Chang et al., 2021), or 299 and 489 Ma (Lutzoni et al., 2018). Within the chytrids, the earliest inferred presence of xyloglucanases is in the common ancestor of Cladochytriales, corresponding to c. 410 Ma (Amses et al., 2022). We note that ancestral state reconstructions have inherent limitations since character states of extinct taxa cannot be considered, and we cannot rule out that xyloglucanases were present in an ancestor common to Dikarya and Chytridiomycota but lost repeatedly among early lineages. Moreover, whether xyloglucanases were gained convergently or by horizontal transfer will require further analysis. In any case, phylogenetic patterns suggest that if xyloglucanases were present in this common ancestor, strong and continuing selection for their conservation only emerged some 250–350 Ma later. Although geological age estimates from dated phylogenies for fungi vary widely, ages of inferred xyloglucanase retention, if not first origin, are estimated to be far younger than the origin of XyG in streptophyte cell walls (Fig. 3).

Fig. 3.

A timeline showing ages of inferred xyloglucan origins in streptophytes and inferred xyloglucanase origins in fungi.

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Timeline showing notable events in plant evolution and inferred xyloglucanase (XyGase) origins in fungi. Though xyloglucan (XyG) may have originated in the streptophyte algae, fungi likely did not evolve xyloglucanases until after land plants evolved. Fungal xyloglucanase evolution may have been driven by vascular plant diversification and the resulting increase in available biomass. Fungal labels represent ages of crown groups. Fungal ages from Chang et al. (2021) and Amses et al. (2022); plant ages from Morris et al. (2018); streptophyte algal ages from Bowles et al. (2024). Vascular plant net diversification rate curve from Silvestro et al. (2015). Organic carbon burial rate curve from Berner (1998), derived from abundance of organic carbon in sedimentary rocks measured in moles per million years. Green dashed arrows represent earliest estimates. LCA, last common ancestor; Ma, million years ago.

We expected that fungi might have been degrading XyG since it first appeared in streptophyte algal cell walls and that inferring xyloglucan‐degrading abilities in ancestral fungi might point to evidence for ancient associations with streptophytes. This was shown to be the case for pectin‐degrading enzymes by Chang et al. (2015), where a common ancestor of Dikarya and Chytridiomycota underwent multiple duplications of pectinase genes, indicative of selection for diversification of these enzymes and of ancient plant–fungus associations. However, we have not found evidence to suggest fungal degradation of XyG before land plant evolution in the gene families analyzed. It has been proposed that XyG might be developmentally dynamic and thus not a substantial component of streptophyte algal cell walls (Popper & Fry, 2003; Mikkelsen et al., 2021); therefore, XyG might not have become abundantly present until later in streptophyte evolution.

What drove the eventual evolution and retention of xyloglucanases in fungi? Opportunities for fungi to use XyG for nutrition and growth may have begun with the global radiation of vascular plants (Silvestro et al., 2015), resulting in a vast increase in biomass where XyG was becoming an increasingly prominent polysaccharide. This increase in plant biomass and diversity, compounded by the complexity and resistance to decay of plant cell walls, is recorded in the fossil record and in the burial of plant‐derived carbon in marine sediments (Berner, 1998; Spencer et al., 2022) starting from the time of plant terrestrialization (515–473 Ma) and continuing through the Carboniferous (c. 300 Ma) (Fig. 3). Accumulation of woody biomass may have supported diversification of fungal enzymes that break down lignin and cellulose (Floudas et al., 2012; Nagy et al., 2016). Similarly, xyloglucanase evolution may have been spurred by land plant innovations like vasculature (450–430 Ma) or seeds (365–330 Ma) (Morris et al., 2018). Opportunities to invade living plant cells may have also played a role in xyloglucanase evolution. In some plant pathogenic fungi, xyloglucanases contribute to the invasion of plants by the breakdown of host cell walls (Rafiei et al., 2021; Jiang et al., 2023). In response, plants evolve to defend themselves by sensing xyloglucanases and initiating immune responses, and the resulting coevolutionary dynamic contributes to pathogen enzyme evolution (Attah et al., 2024).

XyG accumulation in soil could also have served as an energy source for early fungi. Even before the emergence of land plants some 500 Ma, streptophyte algae likely inhabited biological soil crusts (Harholt et al., 2016) and XyG from algal cell walls may have aggregated soil particles, ultimately benefitting early land plants by improving soil properties (Del‐Bem, 2018). Galloway et al. (2018) showed that XyG is secreted from vascular plant roots and liverwort rhizoids, suggesting that the earliest land plants may have increased XyG availability by secretion into the rhizosphere. However, whether fungal enzymes can access XyG adhered to mineral particles remains unknown (Galloway et al., 2018). Xyloglucanases are also found in many soil bacteria (Attia et al., 2018; Attia & Brumer, 2021; Drula et al., 2022), and bacteria would have been competing with fungi for the resource (Wang & Kuzyakov, 2024). Due to questions around access and competition, the importance of the pool of XyG in soil to fungal evolution is largely unknown.

Conclusions

We propose that fungal xyloglucanases evolved in response to quantity and type of plant polysaccharides and that once land plants diversified, fungal enzymes were able to follow suit. We contend that enzymes would have been lost in the absence of selection for their secretion, and so their retention points to their ongoing importance in interactions between two of the great kingdoms of life. We conclude with a few outstanding questions to invite further exploration:

  1. Which putative xyloglucanases function in XyG breakdown? Most of the few experimentally characterized xyloglucanases in fungi are from Ascomycota and Basidiomycota. Functional experiments are needed to test whether bioinformatic predictions of xyloglucanase function hold across the other fungal phyla, separated by hundreds of millions of years of evolution.

  2. Do novel fungal enzymes contribute to XyG breakdown in unexplored fungal phyla? Do xyloglucanases of different evolutionary origin exhibit differential specificity toward cell wall vs secreted XyG, or for the structural diversity found across streptophyte algae and land plants? What would be the specificities of reconstructed, ancestral fungal xyloglucanases? These questions could be approached with transcriptomic studies and functional analysis of substrate specificities of candidate enzymes.

  3. When is XyG degradation important in fungal lifestyle and nutrition? Xyloglucanases likely play a role as virulence factors in plant pathogenicity, but the importance of XyG degradation in nutritional strategies of other fungi, including saprotrophs, ectomycorrhizal fungi, and root endophytes, is unclear.

  4. Are fungal xyloglucanases important in the rhizosphere? Can they access the pool of XyG adhered to soil particles? Ecological roles of xyloglucanases in soil are unknown and will be an interesting area for future study, with implications for soil carbon sequestration.

Competing interests

None declared.

Author contributions

EDT and MLB conceived the topic. EDT carried out analyses, prepared figures and supplementary data files, and led manuscript writing with contributions from HB and MLB.

Acknowledgements

The authors are financially supported by a UBC Four Year Doctoral Fellowship (to EDT) and Discovery Grants from the Natural Sciences and Engineering Research Council of Canada (RGPIN‐2022‐03813 to MLB and RGPIN‐2024‐04318 to HB). The authors thank the consortium of the 1000 Fungal Genomes project, Francis Martin, Rytas Vilgalys, Otto Miettinen, Monika Fischer, Gregory Bonito, Kevin Solomon, and Mariana Kluge for providing access to unpublished genome data. These genome sequence data were generated by the US Department of Energy Joint Genome Institute in collaboration with the user community. The authors acknowledge the use of icons under publication license BioRender.com/r68n580.

Contributor Information

Emily D. Trudeau, Email: emily.trudeau@botany.ubc.ca.

Mary L. Berbee, Email: mary.berbee@botany.ubc.ca.

Data availability

The data that support the findings of this study are available at https://github.com/emdtr/fungal‐xygases.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data that support the findings of this study are available at https://github.com/emdtr/fungal‐xygases.

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